Linking the structure of benthic invertebrate communities and the diet of native and invasive fish species in a brackish water ecosystem
Leili Järv*, Jonne Kotta, Ilmar Kotta & Tiit Raid
Estonian Marine Institute, University of Tartu, Mäealuse 14, EE-12618 Tallinn, Estonia (*corresponding author’s e-mail: [email protected])
Received 14 Dec. 2010, revised version received 16 Feb. 2011, accepted 15 Feb. 2011
Järv, L., Kotta, J., Kotta, I. & Raid, T. 2011: Linking the structure of benthic invertebrate communi-ties and the diet of native and invasive fish species in a brackish water ecosystem. — Ann. Zool. Fennici 48: 129–141.
To date the studies that link community structure of benthic invertebrates with fish feeding are rare as well as factors that are behind this feeding selectivity are poorly known. In this study, we related invertebrate species composition, their dominance structure and fish biological characteristics to the feeding selectivity and overlap of the native flounder, perch and the invasive round goby in Muuga Bay, the Baltic Sea. Spe-cies composition and proportion of benthic invertebrates in the diet of fishes differed from what was available in the field. Except for the round goby, the studied fishes pre-ferred small and mobile invertebrates over large bivalves. However, diet of the studied species, namely the round goby and flounder overlapped. Besides, perch preyed on young stages of the round goby indicating that the introduction of round goby may negatively affect flounder but positively perch.
Introduction
The feeding ecology of fish stands on the two key concepts: Lindeman trophodynamic views (Lindeman 1942) and optimal foraging theory (MacArthur & Pianka 1966). Lindeman’s tro-phodynamic model of ecosystem productivity and energy transfer is the predominant con-ceptual framework that is used to predict the selectivity and transfer efficiencies of lower trophic levels to fuel the production of consum-ers. According to the model, the spatial and tem-poral variability of availability of prey species determines the fluxes of energy/carbon in food webs. Optimal foraging theory, in turn, states that organisms forage in such a way as to maxi-
mize their energy intake per unit time. In other words, organisms are expected to consume food containing the most calories while expending the least amount of time possible in doing so. Thus, prey species are central to both of these models and therefore the generic understanding of fish roles in the ecosystem should be based on sta-tistical relationships between availability of prey species and fish feeding.
The coastal environment of the northern Baltic Sea is characterised by diverse benthic habitats that host many fishes of marine, brack-ish and fresh water origin. Bottom-feeding fishes prevail in the area. Although benthic inverte-brates communities have small number of spe-cies (Kotta et al. 2008b, 2008c), biomass of
130 Järv et al. • ANN. ZOOL. FeNNIcI Vol. 48
invertebrates is high (Kotta et al. 2007, Kotta et al. 2008a) and therefore they provide important source of nutrients to coastal fishes (Ojaveer et al. 1999, Kotta et al. 2009).
Little is known about how fish feeding relates to benthic invertebrate communities in the Baltic Sea ecosystem. Earlier studies demonstrated that food supply is known to affect the species com-position and distribution of fishes (Lappalainen et al. 2000), and availability of benthic inverte-brates is expected to determine fish diet (Lap-palainen et al. 2004). The gut contents analyses showed that the most important and common food of fishes in the northern Baltic Sea were dif-ferent bivalve, gastropod and amphipod species but also insect larvae (Thorman & Wiederholm 1983, Złoch et al. 2005, Kotta et al. 2008b). Fish feeding is known to vary spatially and tempo-rally and is dependent on their growth in length and age (Karås 1987, Licandeo et al. 2006), seasonal changes in temperature (Palomares & Pauly 1998), oxygen (Pihl et al. 1992), light (Dabrowski 1982), and fish morphology (Karl-son et al. 2007). We are not aware of experimen-tal studies that connect fish feeding to their sex and/or maturity stage. There is some circumstan-tial evidence, though, that sex and reproductive status may largely influence feeding behaviour of fish (Lall & Tibbetts 2009). During their ontogenesis fish species often undergo niche shifts involving habitat use and diet (Bergman & Greenberg 1994). Such distribution patterns and behavioural shifts may be gender-specific (Helf-man 1983, Gillanders 1995). In addition, fishes invest energy towards reproduction but this investment likely varies among sexes. Hence, it becomes important to collect dietary information across a range of maturity stages and between sexes. Moreover, earlier studies did not quantifiy in a single framework the links between benthic invertebrate communities and fish diet as well as how fish biological characteristics (including fish maturity and sex) modulate these relation-ships.
Recently, a new fish species, the round goby (Neogobius melanostomus) has been recorded in the northern Baltic Sea. The round goby was first sighted in the region in the Gulf of Riga in 2002 (Ojaveer 2006). Since then the species has dispersed into the Gulf of Finland where it has
formed a self-reproducing population, increased its abundance and colonised new areas. Earlier studies indicated strong competition for space and food among coastal fish communities and invasive species (Kostrzewa & Grabowski 2003, Copp et al. 2005). The round goby is known to have a broad dietary range and therefore it may potentially compete with many native species including flounder and perch. There have been some reports of bioinvasions into the north-ern Baltic Sea involving direct aggression on benthic organisms and/or competition for food and space (Kotta et al. 2001, Kotta & Ólafsson 2003, Kotta et al. 2006, Orav-Kotta et al. 2009). However, we are aware of only one study, where the selectivity of the two most important food items, Macoma balthica and Mytilus trossulus, of round goby and flounder from the experimen-tal/laboratory data were compared (Karlson et al. 2007) but there are no reports on selectivity of those species in field conditions.
In this study, we described the relationships between the biomass dominance structure of benthic invertebrate communities, fish biologi-cal characteristics, the feeding selectivity and dietary overlap of bottom dwelling fishes — flounder, perch and round goby — in Muuga Bay (Gulf of Finland). Our hypotheses were as follows: (1) Biomass structure of benthic inver-tebrates largely determines the variability of fish diet but fish species and size modulate the inver-tebrate–diet relationship. (2) Due to different habitat use and/or varying energy requirements fish diet also varies among different sexes and maturity classes.
Material and methods
Study area
Muuga Bay is located in the central part of the southern coast of the Gulf of Finland, northern Baltic Sea (Fig. 1). Muuga Bay has low water salinity (7–8 PSU) and good water exchange with the open Gulf of Finland. The bottom deposits of the bay include mostly gravel sand and silty sand. The benthic vegetation of Muuga Bay is poorly developed and mainly character-ised by ephemeral algae. Perennial macroalgae
ANN. ZOOL. FeNNIcI Vol. 48 • Benthic invertebrates as the diet of native and invasive fish species 131
and higher plants can be occasionally found in the western parts of the bay. Benthic invertebrate communities have low diversity but the bio-masses are often high (Kotta et al. 2008a).
Test organisms
Flounder (Platichtys flesus) and perch (Perca flu-viatilis) are the dominant fish species in Muuga Bay. Besides the native species, the round goby (Neogobius melanostomus) is a recent ballast water immigrant and exponentially expands its distribution in the area. Flounder is a widely dis-tributed marine species forming a large number of subspecies. The Baltic Sea is populated by P. f. trachurus which has a number of geographical and biological groups. Flounder inhabits mainly sandy or clayey bottoms, younger individuals at smaller depths than older ones. During ontogen-esis the food composition of flounder changes considerably. Larvae feed mostly on phytoplank-ton and different stages of copepods. At the length of 2–3 cm flounder starts consuming benthos and their food markedly differs among areas (Weatherley 1989). Juveniles gradually transfer to the food of adult fish i.e. polychaetes, bivalves, gastropods and even small fish (Vina-gre et al. 2008).
Perch is widely distributed in fresh- and brackish coastal waters preferring shallow, shel-tered and heterogeneous habitats rich in mac-rophytes. Perch is a voracious feeder. Young perch feeds mainly on plankton but also on mysids, gammarids, bivalves, gastropods and small fishes (Pihu et al. 2003). At certain length perch switches on feeding mainly on fishes but they still continue to feed on plankton and ben-thic invertebrates. Perch also preys on the eggs of other fishes (Roots et al. 2004).
Round goby originates from the Ponto-Cas-pian region and is one of the well-known invasive species in the Baltic Sea (Ruiz et al. 1997). The species prefers shallow sandy, gravelly or rocky bottoms with moderate aquatic vegetations. The round goby was observed for the first time in the Estonian waters in 2002. Since 2004 the species is a common inhabitant in Muuga Bay where it has formed a healthy and further expanding popula-tion. The round goby has an aggressive feeding behaviour and feeds mainly on molluscs, smaller fish and fish eggs (Ojaveer 2006).
Sampling and laboratory analyses
Benthic invertebrates were sampled at 13 sam-pling stations in Muuga Bay in July, August and
Fig. 1. Sampling stations of benthic invertebrate communities (filled cir-cles) and fishes (stars) in Muuga Bay.
132 Järv et al. • ANN. ZOOL. FeNNIcI Vol. 48
September 2008 (Fig. 1). Sampling was done with an Ekman type bottom grab (0.02 m2) and one sample was collected from each station. The samples were sieved in the field through 0.25 mm mesh screens. The residuals were stored in a deep freezer at –20 °C and subse-quent sorting, counting and determination of invertebrate species were performed in the lab-oratory using a stereomicroscope. All species were determined to the species level except for oligochaetes, insect larvae and juveniles of gam-marid amphipods. The dry weight of species was obtained after drying the individuals at 60 °C during 48 hours. For the bivalves shell and shell free weights were determined.
Fish sampling was carried out at three stations in July, August and in October 2008 (Fig. 1). At each station, the monitoring gill nets (1.8 ¥ 28.7 m) with mesh sizes of 32, 44, 60, 72, 80, 92, 100 and 120 mm were used. The following parameters were measured: species composition of catches, total length (mm), gape size (maximum height of gape), weight (g), age, sex and maturity stage of all specimens of all species caught by net with given mesh size. Maturity stage was determined according to a routine six-point macroscopic maturity scale: immature (I), maturing (II–IV), running (V) and spent (VI). This classification is based on the degree of clasper calcification, and development of testes and reproductive ducts for males and on the condition of uteri, oviducal glands and ovar-ian follicles for females (Anon. 2007: 9–10). In addition food composition of flounder, perch and round goby were assessed. In order to determine the food composition of fishes their stomach content was fixed immediately after catching in 70% alcohol. The quantitative composition of stomach contents was determined in the labora-tory using a similar procedure as above.
Data analyses
Multivariate data analyses were performed with the statistical program “PRIMER” ver. 6.1.5 (Clarke & Gorley 2006). Prior to analyses, all distribution data were standardized by dividing biomass values of each invertebrate species by total invertebrate biomasses of the respective
station. Similarly, the gut content data were standardized by dividing the biomass values of invertebrate species eaten by the total biomass of the gut content. Similarities between each pair of samples were calculated using a zero-adjusted Bray Curtis coefficient. The coefficient is known to outperform most other similarity measures and enables samples containing no organisms at all to be included (Clarke et al. 2006). A non-metric multidimensional scaling analysis (MDS) on macrobenthic biomasses was used to visualize the dissimilarities in the community composition of benthic invertebrates within gut of different fish species. Statistical differences in benthic invertebrate communities and fish diet were assessed by the ANOSIM permutation test (Clarke 1993). A BEST analysis (BIOENV procedure) was used to relate the fish charac-teristics such as species, length, weight, sex, maturity and age to the gut content of fish. The variables of fish characteristics were normal-ized prior to analyses. The analysis shows which fish characteristic (or combination of different characteristics) best predicts the observed feed-ing pattern. A Spearman rank correlation (r) was computed between the similarity matrices of fish characteristics and gut content. A global BEST match permutation test was run to examine the statistical significance of observed relationships.
In order to standardize fish feeding among species, regressions between body length and the gape size (maximum height of gape) of fishes were found (Karlson et al. 2007). The fit of the linear regression models was generally good (round goby: r2 = 0.955, F1,29 = 597.21, p < 0.0001; flounder: r2 = 0.955, F1,29 = 597.21, p < 0.0001; perch: r2 = 0.954, F1,27 = 589.87, p < 0.0001). The relationships between body length and gape size classes is presented in Table 1.
The Manly-Chesson index α (Manly 1974, Chesson 1978, 1983) was calculated to evaluate prey selection. The index formula is as follows:
with ri = the proportion of food item i in the diet and pi = the proportion of food item i in the environment, m = the number of food items in the environment. The values of α range from 0
ANN. ZOOL. FeNNIcI Vol. 48 • Benthic invertebrates as the diet of native and invasive fish species 133
(complete avoidance) to 1 (complete preference). If α = 1/m, the predator is feeding randomly and the preys are consumed in proportion to abun-dance in environment, whereas α > 1/m indicates preference and α < 1/m indicates avoidance. The shell-free biomass was used to calculate fish feeding selectivity and the contribution of differ-ent benthic invertebrates to fish diet.
The diet overlap between the studied species was estimated using Morisita’s index (C) (Horn 1966, Cortés 1997):
where Xi and Yi are the proportions of the ith food category in the diet of species X and Y, respec-tively. The values close to zero suggest large dis-similarities in the diet, and the values close to 1 represent similar stomach contents. According to Zaret and Rand (1971), the overlap ≥ 0.6 results in strong competitive interactions among species.
Results
Altogether 26 taxa of infaunal and epifaunal invertebrates were collected from Muuga Bay (Table 2). The available benthic food resource in the area was clearly dominated by bivalves, par-ticularly Macoma balthica and Mytilus trossulus and these species constituted 65% and 24% of
Table 1. Gape size classes (mm) and corresponding total lengths (mm) of round goby, flounder and perch. The defined gape size classes are as follows: small gape size ≤ 14.5 mm, medium 14.6–17.0, large > 17.0. The sample sizes are given in parentheses.
total dry biomass, respectively. When excluding shell weight, the bivalve species contributed 45% and 15% and the crustacean Palaemon adspersus 25% of total biomass, respectively. The cirriped Balanus improvisus and the bivalves Mya are-naria and Cerastoderma glaucum had elevated biomasses only at some stations. The biomass of other taxa did not exceed 1% of the total biomass.
The gut content analyses indicated that floun-der and perch mainly fed on benthic inverte-brates and to a lesser extent on other food items (Table 3). Altogether 8 benthic invertebrate taxa were found in the stomach samples, including
some of the most dominant species. The food spectra of benthic invertebrate species did not match the availability of prey. ANOSIM showed large differences between the species composi-tion of benthic invertebrate communities and those consumed by fishes. Except for the dif-ferences in the gut content between perch and flounder, the composition of gut content signifi-cantly varied among fish species (Table 4).
Similarly, the proportion of benthic inver-tebrates in the diet of fishes differed from what was available in the field and the proportions of different food items in diet differed statistically among fish species (Table 5). Flounder preyed less on M. trossulus and M. balthica and more on Hydrobia spp. and Hediste diversicolor than was expected from their proportions in the field. Similarly, perch consumed less M. trossulus, M. balthica but also P. adspersus and more Hydro-bia spp., Neomysis integer, H. diversicolor and Gammarus spp. than was expected from their proportions in the field. The round goby pre-ferred M. trossulus, Hydrobia spp. and H. diver-sicolor over M. balthica.
However, as indicated by low distances among groups (i.e. within group variability was not much smaller that between group variability; see the r values in Table 4), the diet of the studied
Table 3. composition of fish diet by gape size classes (% of invertebrate taxa in the total stomach content, bivalves’ shell dry weight excluded). The diet composition was calculated taking into account only stomachs that contained food. The defined gape size classes are as follows: small gape size ≤ 14.5 mm, medium 14.6–17.0, large > 17.0.
Flounder Round goby Perch Small Medium Large Small Medium Large Small Medium Large
Table 4. Differences in the species composition of benthic invertebrates between the field and the guts of different fish species as well as between the guts of dif-ferent fish species as evidenced by ANOSIM. Permuta-tion/randomisation methods on the resemblance matrix (the actual number of permutation 999) were used.
Pairwise tests r p
Round goby vs. Flounder 0.072 < 0.001Round goby vs. Perch 0.123 < 0.001Round goby vs. Availability of prey 0.932 < 0.001Flounder vs. Perch 0.050 0.057Flounder vs. Availability of prey 0.954 < 0.001Perch vs. Availability of prey 0.967 < 0.001
ANN. ZOOL. FeNNIcI Vol. 48 • Benthic invertebrates as the diet of native and invasive fish species 135
species largely overlapped. This is also shown by the MDS ordination of fish stomach contents (Fig. 2). Round goby had the largest variability in the stomach content whereas variability in the stomach content of flounder was the smallest.
The BEST permutation analysis demon-strated that besides the biomass structure of benthic invertebrate communities, the stomach content of fish was explained by the separate effect of fish weight and age and to a lesser extent by fish length, maturity and sex. However, when both fish weight and age were included into models, fish length, maturity and sex did not explain additional variability of the models of fish feeding (Table 6).
Similar to the multivariate ANOSIM analy-sis, the Manly-Chesson index gave analogous preferences of benthic invertebrates in the diet of fishes with strong interspecific and size effects (Fig. 3). Likewise, the multivariate MDS analy-sis, the univariate comparison of feeding spectra showed a considerable overlapping between all size groups of the round goby and young (100–120 mm) flounder (IM = 0.64 ± 0.1). The over-lapping between feeding spectra of round goby and > 250 mm flounder was considerably lower (IM = 0.32 ± 0.12). The dietary overlap between
Table 6. Relationship between the fish characteristics and the gut content of fish (BeST analysis, BIOeNV procedure, p < 0.01 i.e. the number of permuted sta-tistics greater than or equal to r was 0). r denotes a Spearman rank correlation between the similarity matri-ces of fish characteristics and gut content.
Variables r
Separate contribution Species 0.168 Length 0.120 Gape size 0.026 Weight 0.142 Age 0.130 Sex 0.012 Maturity 0.018Best results Species ¥ Weight ¥ Age 0.346 Species ¥ Weight 0.178
Table 5. Differences in the biomass dominance of ben-thic invertebrate species between the field and the guts of different fish species as well as between the guts of different fish species as evidenced by ANOSIM. Per-mutation/randomisation methods on the resemblance matrix (the actual number of permutation 999) were used.
Pairwise tests r p
Round goby vs. Flounder 0.079 < 0.001Round goby vs. Perch 0.130 < 0.001Round goby vs. Availability of prey 0.210 0.021Flounder vs. Perch 0.057 0.039Flounder vs. Availability of prey 0.355 < 0.002Perch vs. Availability of prey 0.491 < 0.001
Round goby
Flounder
Perch
2D Stress: 0.02
Fig. 2. MDS ordination of biomasses of benthic invertebrate species in the stomach of fishes.
136 Järv et al. • ANN. ZOOL. FeNNIcI Vol. 48
Fig. 3. Manly-chesson selection index (mini-mum, mean, maximum) of main food items for (a) small perch, flounder and round goby (gape size ≤ 14.5 mm), (b) medium perch, flounder and round goby (gape size 14.6–17.0 mm), and (c) large perch, flounder and round goby (gape size > 17.0 mm). Values above the dashed line indicate preference, values on the line refer to proportional intake and values below the line show avoidance of prey.
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
ROUND GOBYPERCH
a
b
c
FLOUNDER
Man
ly-C
hess
on in
dex
0
0.2
0.4
0.6
0.8
1Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
ROUND GOBYPERCH FLOUNDER
Man
ly-C
hess
on in
dex
0
0.2
0.4
0.6
0.8
1
Man
ly-C
hess
on in
dex
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
Mytilus
Macoma
Hydobia
Hediste
Neomysis
Gammarus
Corophium
Palaemon
ROUND GOBYPERCH
0
0.2
0.4
0.6
0.8
1
FLOUNDER
80–150 mm perch and 120–140 mm round goby was also low (IM = 0.31 ± 0.16) (Table 7). Only
flounder and perch preyed to a large extent on different food items.
ANN. ZOOL. FeNNIcI Vol. 48 • Benthic invertebrates as the diet of native and invasive fish species 137
Discussion
We predicted that biomass structure of benthic invertebrates largely determines the variability of fish diet (first part of hypothesis 1). Our study did not conform the hypothesis as fish diet was only weakly associated with the availability of prey in the field. Therefore, our study gives further evidence that the studied fish species are highly selective (Ghedotti et al. 1995, Aarnio & Bondorff 1997, Adamek et al. 2004, Truemper & Lauer 2004, Andersen et al. 2005).
The results also indicate that food availability is likely not a limiting factor in the growth of founder and perch but may limit the growth of round goby. The bivalves Mytilus trossulus and Macoma balthica were the two of main food items for the studied fishes and only round goby preyed on M. trossulus more than was expected from their proportions in the field, i.e. had a potential to reduce the relative biomass of the prey species.
We also predicted that the selectivity of fish varied among species (second part of hypoth-esis 1). Our data supported the hypothesis except for significant overlap of diet between round goby and small flounder. Although some authors reported broad dietary overlap among estuarine fishes (Ley et al. 1994), our findings suggest that food partitioning is the main coexistence mechanism in the study area regardless of high invertebrate biomasses. Fishes that avoid dietary overlapping avoid competition.
We also predicted that fish diet varied with size as it is expected that the gape size of fish is related to its length (second part of hypoth-esis 1). Our analyses showed that fish weight and age largely modified the feeding of fishes, espe-
cially that of flounder and perch. The diet com-position of flounder clearly reflected the physical capabilities of fish to swallow the prey, support-ing the conclusion of Karlson et al. (2007) that the size of the food items depends on the width of mouth.
Finally, we predicted that fish diet varied with sex and maturity class (hypothesis 2). Our data did not support the hypothesis. Instead, the analyses showed that the dependence of fish diet on sex and maturity was largely modulated by fish length and weight. This agrees with the findings of earlier studies performed outside the Baltic Sea area with no relationship between fish sex, maturity stage and diet composition (e.g. Barbini et al. 2010, Powter et al. 2010). The significant effects of sex on fish feeding are only expected when the analyses are performed separately for different size classes. Such finding is also supported by previous feeding studies of many fish species including white bream, bream, perch and others (Wielgosz & Tadajewska 1988, Wziątek et al. 2004).
The gut content analyses showed that floun-der had both low individual feeding variability (difference in gut content among individuals) and low overall feeding diversity (number of species preyed). This indicates that flounder is a specialist feeder with a small niche width. Round goby in turn was characterised by both high feeding variability and diversity, i.e. generalist feeding strategy. Perch had the broadest feeding spectra (high feeding diversity) but moderate feeding variability and therefore is an oppor-tunistic feeder that feeds on all exposed items (Fishelson 1977, Mavuti et al. 2004). However, as perch switches from invertebrate food to other prey already at very young stages (Leach
Table 7. Average Morisita index (± Se) of dietary overlap (IM) by fish species and their gape size classes. The defined gape size classes are as follows: small gape size ≤ 14.5 mm, medium 14.6–17.0, large > 17.0.
Small round goby Medium round goby Large round goby
et al. 1997) the species is not so much depend-ent on the availability of benthic invertebrates as compared with flounder and round goby. Our results clearly demonstrated that perch can prey on young stages of fishes including the round goby. Flexibility in the feeding behaviour of perch and round goby enables them to efficiently utilize the available food and give them a com-petitive advantage over specialized feeder in the dynamic ecosystems of the Baltic Sea (Mavuti et al. 2004, Balshine et al. 2005).
The coexistence of species in the communi-ties is primarily regulated by the competition for food and space (Schoener 1974, Ross 1986). Introduction of a new species potentially inten-sifies competitive interactions and may desta-bilize native communities. Stronger effects are expected in young ecosystems such as the Baltic Sea (Balshine et al. 2005). The round goby, invading with ballast waters, has shown itself a successful competitor in a number of water-bodies such as the US Great Lakes (Jude et al. 1992), Gdansk Bay (Leppäkoski et al. 2002), and Curonian Bay (Rakauskas et al. 2008) just to name a few. The evidence from Great Lakes shows that round goby successfully outcompetes yellow perch (Perca flavescens), close relative of European perch, both for space and food (John 2001). Similarly it has been shown that the abundant population of the round goby depleted benthic fauna in Gdansk Bay (Skóra & Rzeźnik 2001). It is interesting to note that although Karlson et al. (2007) carried out their study in the laboratory and our study is based on the field observations, the patterns found in both studies were exactly the same, namely diets of small flounder and round goby overlap significantly. Thus, based on earlier evidence and the results of our study, round goby is expected to compete with young flounder in the coastal zone of the northern Baltic Sea including Muuga Bay (Karl-son et al. 2007). On the other hand, our results also show that perch can prey on young stages of round goby. Thus, abundant European perch population can potentially control the population growth of round goby in the study area since the share of the invasive species in the diet of perch is expected to increase with further expansion of round goby. This indicates that the introduction of round goby may negatively affect flounder but
positively perch (Almqvist et al. 2010).In addition to interspecific interactions, the
invasion of round goby may have a positive implication from a food-web efficiency point of view. Namely, round goby was the only studied fish species that consumed proportionally more deposit and suspension feeding bivalves than was expected from their proportions in the field. Being itself eaten by perch, round goby increases trophic transfer of bivalves up the food chain (Almqvist et al. 2010). The northern Baltic Sea is characterised by high benthic secondary pro-duction but low benthivorous fish biomass and therefore these trophic groups are largely not consumed by predators but rather channelled into the detritus food chain (Tomczak et al. 2009).
Conclusions
1. The food spectra of benthic invertebrate spe-cies did not match the availability of prey but was influenced by fish species and size.
2. Except for round goby, the studied fish spe-cies preferred small and mobile invertebrates over large bivalves.
3. Despite of many significant differences, diet of the studied species somewhat overlapped with round goby having the largest and flounder having the smallest variability in its stomach content.
4. The study suggests that food availability is likely not a limiting factor in the growth of founder and perch but may be important for round goby.
5. Introduction of round goby may negatively affect flounder but positively affect perch and therefore perch may potential control the population growth of the round goby in the study area. The validity of such hypotheses, however, should be tested in future experi-mental studies.
Acknowledgements
Funding for this research was provided by target financed project SF0180013s08 of the Estonian Ministry of Education and Research, by the Estonian Science Foundation grants 7813, 8254, the EU FP7 project VECTORS (grant agreement 266445) and by the Port of Tallinn.
ANN. ZOOL. FeNNIcI Vol. 48 • Benthic invertebrates as the diet of native and invasive fish species 139
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